Lindy Ruff dreamed of holding the Stanley Cup in his adopted town of Buffalo. He pictured himself skating around Memorial Auditorium with the chalice over his head. He envisioned himself clutching the Cup on the bench in First Niagara Center.

He held onto the dream for half of his life. Now he has to let it go.

Ruff’s run in Blue and Gold came to an end Wednesday when the Sabres fired the longest-tenured coach in the NHL. Ruff, who turned 53 on Sunday, spent 26 years in the Sabres’ organization. He coached the team for the last 16 years and also played in Buffalo for a decade.

The lengthy, memorable ride came to its conclusion with the Sabres near the bottom of the league with a 6-10-1 record.

“First and foremost, I would like to thank Lindy as a player, as a great coach and an outstanding citizen in this community and for all the work that he has done for the organization,” said Darcy Regier, who hired Ruff on July 21, 1997, just a month after becoming general manager. “Unfortunately, the coaches too often pay the price. It’s something that I not only avoided but made every effort to avoid in the past.”

The decision had become unavoidable, however. Even Ruff’s closest friends could see it.

Larry Playfair skated alongside Ruff for seven seasons with the Sabres, beginning in Ruff’s rookie year of 1979-80. Playfair also worked with Ruff often as the president of the Sabres’ alumni association.

He sensed their time together in the organization was coming to an end following an uninspired 2-1 loss to Winnipeg on Tuesday night.

“I watched Lindy’s press conference after the game, and it’s as down as I’ve seen him in a long, long time,” Playfair said Wednesday night in First Niagara Center during a Junior Sabres game. “I don’t typically do it, but this morning I watched it again on Sabres.com. You can just see he’s tried everything he can try and the guys aren’t responding. If he’s out of answers, I look at it as maybe my friend Lindy Ruff gets a break now.

“I know he came here in hopes of winning a Stanley Cup. I think he put a lot, lot more pressure on himself than anybody else did. I’m thinking maybe this might be just a chance for him to catch his breath.”

Ruff will no doubt get another opportunity to coach in the NHL. He’ll bring a resume filled with accomplishments and disappointments.

Named Coach of the Year in 2005-06, Ruff holds the Sabres’ record for most wins (571) and games coached (1,165). Those totals are second only to Al Arbour for most with a single franchise. Arbour coached the New York Islanders to 740 victories in 1,500 games.

“I think back to the interview,” Regier said while choking back tears. “I called Scotty Bowman about him. I said, ‘Scotty, who would you compare him to?’ And he said, ‘Darcy, he’s a lot like Al Arbour,’ for you older fans here, ‘with a sense of humor.’ I think Scotty was right.”

Ruff guided the Sabres to four Eastern Conference finals appearances (1998, 1999, 2006, 2007), and they went for the Cup against Dallas in 1999 but lost in six games. He also appeared in the conference finals as a rookie before losing to the Islanders, one of seven trips to the postseason as a player.

He asked for a trade in 1988-89 but returned for his first head coaching opportunity after four seasons as an assistant in Florida.

“It was intriguing to him to come back to Buffalo,” Playfair said. “He played here. He was the captain of our team here. We never won.

“He went on and got involved in coaching and then got the opportunity. I think he looked at it as, ‘You know what? I didn’t win as a player, but maybe we can pull this off as a coach.’ Boy, he came close.”

The Sabres won the Presidents’ Trophy as the NHL’s top team in 2006-07. Before falling to Ottawa in the conference finals, they beat the Islanders and New York Rangers. They were Ruff’s final postseason victories.

Ruff and the Sabres have missed the playoffs three of the last five years. They also lost in the first round to Boston (2010) and Philadelphia (2011). They sat home during the postseason in six of Ruff’s 14 seasons and were on their way toward doing it again.

“As a coach he can be demanding, but he cares a lot,” goaltender Ryan Miller said by phone from Toronto, where the Sabres play tonight. “That’s what you want. You want somebody there who cares, is going to put the time in and be professional.

“I don’t have any doubts that Lindy’s not done coaching. Certainly, his career will continue somewhere else. It’s just unfortunate that the organization he cares so deeply about has to end.”

Although Ruff had immediate success behind the bench, including four straight playoff appearances, he initially had naysayers because he replaced popular Coach of the Year Ted Nolan. Ruff won most of them over with his quick wit, intense attitude and designer suits and ties.

“He’s been the face of the team for a long time,” said retired defenseman Jay McKee, who played nine seasons under Ruff. “I respect him tremendously. He was a guy that not only was the coach here for a long time, but he played here. He’s just a legendary figure as a Buffalo Sabre.”

Ruff’s demeanor changed this year. Players expressed displeasure with his public criticisms at the end of last season, so the coach eased up.

“He was actually more fiery in his younger years,” McKee said. “I wouldn’t say he got soft. He still has an edge and brings it out, but it’s not all the time. He picks his spots maybe a little bit more than he used to during my career with him.”

The change didn’t work. The Sabres kept losing no matter which Ruff showed up for meetings and news conferences.

“He didn’t lose the team in any way with respect to communication,” Regier said. “In fact, communication has never been better. There were huge strides done in that regard.

“Unfortunately in this case, that change I think created a risk that didn’t pay off.”

Ruff’s career with the Sabres is over, but it’s unlikely his time in the area is finished. His four children grew up in Western New York, and his son Brian plays for the Junior Sabres. The Alberta native became a Buffalo guy.

So although his dream of bringing the Stanley Cup to town has ended, it won’t fade easily. He’s been carrying it for too long.

“My guess is wherever Lindy Ruff ends up going,” Playfair said, “Buffalo will still be a big part of his life.”